Larval Development of Etropus Longimanus (Paralichthyidae) and Symphurus Trewavasae (Cynoglossidae) Off the Buenos Aires Coast, Argentina

Scientia Marina 76(1) March 2012, 29-37, Barcelona (Spain) ISSN: 0214-8358 doi: 10.3989/scimar.2012.76n1029

Larval development of Etropus longimanus (Paralichthyidae) and Symphurus trewavasae (Cynoglossidae) off the Buenos Aires coast, Argentina

CARLA DERISIO 1,2, PAOLA BETTI 1,2, JUAN MARTIN DIAZ DE ASTARLOA 2,3 and LAURA MACHINANDIARENA 1 1 Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP) PO Box 175, B7602HSA Mar del Plata, Buenos Aires, Argentina. 2 Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Rivadavia 1917, 1033 Buenos Aires, Argentina. 3 Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Funes 3350, B7602AYL Mar del Plata, Buenos Aires, Argentina.

SUMMARY: The larval development of Etropus longimanus and Symphurus trewavasae (Pleuronectiformes) off the Buenos Aires coast was described. Both species have an elongated body; however, as the total length of Etropus longimanus larvae increased, their body became deeper. In Symphurus trewavasae the intestine was noticeably coiled. In E. longimanus the notochord flexion started at 3.9 mm and was completed at 5.0 mm standard length (SL). Vertebral formation began in larvae with a 4.6 mm SL and the definitive number of vertebrae (34-39) was observed in larvae of 4.8 mm SL. The dorsal fin had two elongated rays and the pelvic fins had only one. In Symphurus trewavasae the notochord flexion began at 5.9 mm and was completed at 8.0 mm SL. Migration of the right eye was completed in the metamorphic stage at 10.5 mm SL. Vertebral column ossification finished in flexion larvae of 6-7 mm SL, with a total number of 48-50 vertebrae. Four elongated rays of similar length were observed on the dorsal fin. Keywords: Pleuronectiformes, early development, larvae, flatfish, tonguefish, SW Atlantic.

RESUMEN: Desarrollo larval de Etropus longimanus (Paralichthyidae) y Symphurus trewavasae (Cynoglossidae) en la costa Bonaerense, Argentina. – Se describe el desarrollo larvario de Etropus longimanus y Symphurus trewavasae (Pleuronectiformes) que habitan la costa de Buenos Aires. El cuerpo de las larvas de ambas especies es alargado, pero en Etropus longimanus la altura del cuerpo se incrementa con el crecimiento. El tubo digestivo de Symphurus trewavasae es considerablemente enrollado. La flexión del urostilo en larvas de E. longimanus se inició cerca de los 3.9 mm y finalizó cerca de los 5 mm de longitud estándar (LS). Se observaron vértebras definidas en larvas de 4.6 mm LS y el número definitivo (34- 39) se visualizó en individuos de 4.8 mm LS. Se distinguen dos radios largos al inicio de la aleta dorsal y uno en la pélvica. En Symphurus trewavasae la flexión del urostilo comenzó cerca de los 5.9 mm LS y finalizó aproximadamente a los 8.0 mm LS. La migración del ojo derecho hacia el lado izquierdo de la cabeza finalizó en el estadio de metamorfosis (10.5 mm LS). La osificación de la columna vertebral se completó en larvas entre los 6 y 7 mm LS, con un número total de 48-59 vértebras. Al inicio de la aleta dorsal se distinguen 4 radios largos con igual longitud. Palabras clave: Pleuronectiformes, desarrollo temprano, larvas, lenguado, lengüita, Atlántico Sudoccitental.

INTRODUCTION tween 34° and 47°S (Fabré and Díaz de Astarloa 1996), and form large concentration areas in the Argentinean- In the southwestern Atlantic Ocean the order Pleu- Uruguayan Common Fishing Zone (AUCFZ) (Fabré ronectiformes is represented by more than 20 flatfish and Díaz de Astarloa 2001). There is one species of species (Menni et al. 1984) that mainly inhabit be- Etropus (Paralichthyidae) and two species of Symphu- 30 • C. DERISIO et al. rus (Cynoglossidae) on the Argentine continental shelf (Cousseau and Denegri 1997, Munroe 1998). Etropus longimanus (Norman 1933) is a small- sized flatfish (maximum reported size is 155 mm) oc- curring on soft bottoms, from the coastline to 190 m depths, and is one of the five paralichthyid species that inhabit the area. It occurs from Cabo Frio (Brazil) as far south as northern Patagonia, Argentina (Figueiredo and Menezes 2000). It has no commercial importance because of its small average size and low abundance compared to the other paralichthyid flatfishes caught in the area, such as Paralichthys orbignyanus, P. isos- celes, P. patagonicus and Xystreurys rasile (Díaz de Astarloa 2002). The tonguefish Symphurus trewavasae (Chabanaud 1948) is also a small-sized species reported to attain a maximum size of ca. 139 mm (Menezes and Benvegnu 1976). 85% of the specimens were collected by Mun- roe (1998) in the southwestern Atlantic inner continental shelf from southeastern Brazil to central Argentina. It has no commercial importance. Kurtz and Matsuura (1994) described the development of S. trewavasae off the Brazilian continental shelf. Larvae of Etropus are difficult to distinguish and are often ignored or classified as “unidentified bothids” in species composition analyses. Moreover, there is no information on the early life cycle of pleuronectiforms in the Argentine Sea. Therefore, in this paper we described the larval development of the flatfish Etropus longimanus and the tonguefish Symphurus trewavasae collected off Buenos Aires.

MATERIALS AND METHODS Fig. 1. – Etropus longimanus larval development: (a): preflexion larvae (2.8 mm NL); (b): larvae in flexion (4.9 mm SL) and (c): A total of 153 fish larvae of Etropus longimanus postflexion larvae (8.9 mm SL). and 33 of Symphurus trewavasae were collected during research cruises conducted by INIDEP (Instituto Na- HL or SL, y is the morphometric measurement under cional de Investigation y Desarrollo Pesquero) in 1998, analysis, a the intercept (expected value of y at x = 1) 2000 and 2001 at a fixed station (36°28’S 54°48’W). and b the slope. The confidence intervals (at the 95% Samples were taken with a Bongo net with a 300 and significance level) of the allometric parameter were 500 μm mesh size and a Nackthai net, a German modi- calculated. In addition, each morphometric measure- fication of the Gulf V high speed sampler (Nellen and ment was calculated as a proportion of SL (morpho- Hempel 1969), with a 400 μm mesh size. Ichthyoplank- metric index, I %). ton samples were fixed in a solution of 5% formalin to Thirty-eight larvae of Etropus longimanus and 18 seawater. of Symphurus trewavasae were cleared and double The following measurements were recorded ac- stained with alcian blue for cartilage and alizarin red cording to Neira et al. (1998): body length (BL), for bone, according to Potthoff (1984) and Taylor notochord length (NL), standard length (SL), body and Van Dyke (1985), and then examined for mer- depth (BD), eye diameter (ED), head length (HL), istic and osteological features. Whenever possible, head depth (HD), preanal length (PAL), and predorsal the number of vertebrae and fin rays were recorded. length (PDL). Preserved larvae were measured to the The total number of myomeres was also counted. In nearest 0.1 mm with an ocular micrometer fitted to S. trewavasae larvae, the number of dorsal pterygi- a dissecting microscope. Shrinkage was not consid- ophores inserting into the first five interneural spaces ered in the measurements. Specimens were divided was recorded as the interdigitation pattern according into developmental stages according to Sumida et al. to Munroe (1992). Pigmentation pattern, morphomet- (1979). ric, meristic and osteological features were analyzed The equation y = a xb was applied to determine on the left side of the body. The different develop- whether the different body parts have allometric or mental stages were illustrated according to Trnski and isometric growth in relation to SL or HL, where x is Leis (1991).

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RESULTS the body (Fig. 1a). Three or four internal pigments also appeared along the notochordal line between myomers Etropus longimanus 24 and 27 (Fig. 1a). Notochord flexion was completed at 5.0 mm SL General morphological features and pigmentation (flexion stage, 4.2-5.3 mm SL). During the flexion stage, larvae became more pigmented. Internal noto- The smallest larva collected was 2.8 mm NL. Dur- chordal pigment consisted in a series of 11 stellated ing the preflexion stage (2.8-4.2 mm NL) the larval chromatophores between the gas bladder and myomer body was relatively elongated, but as the body size 27 (Fig. 1b). increased in length, larvae became deeper bodied (Fig. The biggest individual that was collected was 10.5 1a). Three to five internal melanophores appeared mm SL. During the postflexion stage (5.5-10.5 mm SL), above the hindbrain and small external ones along the there were two dash-like clusters of pigment along the lower and upper jaws (Fig. 1a-c). There were several ventral margin of the tail between myomers 20-23 and melanophores along the ventral and lateral surface of 27-35, and there was a series of small melanophores the abdomen, so that pigmentation increased with lar- along the distal tips of anal pterygiophores (Fig. 1c). val size (Fig. 1a-c). There were small melanophores at Less melanophores were observed on the anterior region the base of the pectoral fin. The gas bladder was heav- of the ventral margin, with the consequent formation of ily pigmented, with four or five distinct melanophores two main groups. The first group was constituted by four (Fig. 1a-c). melanophores located very close to the middle of the At the preflexion stage, there were two dash-like ventral body margin, and the second group (separated clusters of pigment along the dorsal margin of the from the first group by three myomers) was composed tail between myomers 6-11 and 23-31 (Fig. 1a). One of nine melanophores that almost reached the end of the melanophore per myomer (from myomer 8 to 38 ap- anal fin (Fig. 1c). There were a few melanophores be- proximately) was observed on the midventral line of fore the base of the pelvic fin (Fig. 1c).

Fig. 2. – Regression between (a): body depth (BD); (b): head length (HL); (c): head depth (HD); (d): preanal length (PAL) and notochordal length (NL) or standard length (SL); and between (e): head depth (HD); (f): eye diameter (ED) and head length (HL) of Etropus longimanus larvae. Values in parenthesis are 95% CI of the slope.

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Table 1. – Morphometric index (I%) calculated for Etropus longimanus and Symphurus trewavasae. BD: body depth; HD: head depth; HL: head length; NL: notochordal length; n: number of measurements; PAL: preanal length; SL: standard length. Etropus longimanus Symphurus trewavasae NL or SL HL HD BD PAL (mm) I % n I % n I % n I % n 2.0 22.9 5 28.6 5 28.0 5 55.5 2 3.0 24.3 39 28.3 39 27.6 39 43.6 8 4.0 25.5 51 30.5 56 31.4 52 46.3 6 5.0 27.3 11 32.6 11 34.5 11 44.7 5 6.0 29.0 11 33.7 11 36.1 9 47.3 4 7.0 28.2 13 30.8 13 36.6 12 44.2 3 8.0 27.5 11 29.5 11 37.4 11 39.4 3 9.0 28.2 2 27.3 2 40.9 2 39.3 1 10.0 27.0 5 28.0 5 40.7 5 32.4 1

Etropus longimanus larvae were moderately sequently, HL remained approximately constant elongate at the beginning of their development. (Table 1). HD showed a positive allometric growth Table 1 shows the indices related to SL that most pattern with respect to SL (P<0.05) (Fig. 2c). It in- clearly indicate body transformation, and Fig. 2 creased from 28.5% NL to 33.7% SL in fish larvae shows the morphometric regressions. BD showed up to 6 mm SL and then decreased to 28% SL in a positive allometric growth pattern with respect to larvae of 10 mm SL (Table 1). HD showed a nega- SL (P<0.01), increasing from 27.5% NL to 41% SL tive allometric growth pattern with respect to HL (Fig. 2a, Table 1). HL increased in relation to SL, (P<0.01) (Fig. 2e). PAL (Fig. 2d) increased isomet- also following a positive allometric growth pattern rically with respect to the SL (P>0.05). ED showed (P<0.01) (Fig. 2b), increasing from 23% NL to 29% a negative allometric growth pattern in relation to SL in fish larvae up to 6 mm SL (Table 1). Sub- HL (P<0.01, Fig. 2f).

Table 2. – Sequence of appearance and number of myomeres, vertebrae and fin rays of Etropus longimanus larvae. Body length (mm) Larval stages Total myomeres Total vertebrae Dorsal rays Anal rays Pelvic rays Caudal rays 2.8 Preflexion 37 2 15 1 3.1 Preflexion 2 3.2 Preflexion 35 2 3.3 Preflexion 36 2 3.3 Preflexion 37 2 1 3.3 Preflexion 41 2 1 3.3 Preflexion 38 2 3.3 Preflexion 37 2 3.5 Preflexion 34 2 3.7 Preflexion 38 2 3.8 Preflexion 38 2 1 3.9 Preflexion 39 2 3.9 Preflexion 37 2 4.2 Preflexion 33 2 3 4.2 Preflexion 34 2 1 4.2 Flexion 2 4.5 Flexion 36 44 35 1 12 4.6 Flexion 38 38 44 25 3 12 4.6 Flexion 2 4.7 Flexion 37 52 4.8 Flexion 37 20 21 7 4 10 4.8 Flexion 36 36 69 53 1 17 5.0 Flexion 36 29 22 1 10 5.1 Flexion 37 63 49 4 11 5.5 Postflexion 36 36 70 51 6 17 6.1 Postflexion 35 35 73 59 4 17 6.3 Postflexion 36 36 70 54 6 17 6.5 Postflexion 37 37 75 65 6 17 7.3 Postflexion 38 38 73 56 6 17 8.0 Postflexion 39 39 70 57 6 17 8.0 Postflexion 35 35 73 60 6 16 8.0 Postflexion 35 35 75 66 6 17 8.1 Postflexion 36 36 65 54 6 17 8.1 Postflexion 35 35 75 60 6 17 8.3 Postflexion 34 34 68 64 6 17 8.3 Postflexion 36 36 74 66 6 17 8.9 Postflexion 34 34 77 59 6 17 9.1 Postflexion 34 34 74 61 6 17

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Fig. 3. – Sequence of the development of morphological characters in early life stages of Etropus longim in relation to notochordal length (NL) or standard length (SL): start of development of the character ( ); appearance of fin rays ( ); character completely developed ( ). Pref. S.: preflexion stage; F. S.: flexion stage. Fins and meristic features

33 to 41 myomers were observed from the beginning of the preflexion stage. Vertebral ossification began in the flexion stage (4.6 mm SL) (Table 2). Os- sification started from the head towards the posterior part of the body and the definitive number of vertebrae (34-39, without urostyle) was observed in larvae of 4.8 mm SL (flexion stage) (Fig. 3, Table 2).

Fin development

In preflexion larvae, finfolds and pectoral fin buds were the first parts of the fins observed. The finfold was gradually lost as the other fins developed (Fig. 1, Fig. 3). The development of the dorsal fin began at the preflexion stage (2.8 mm SL) (Fig. 3). It had two elongated rays that remained during all larval developmental stages (Table 2). The dorsal fin attained the final number of rays at the beginning of the postflexion stage (69-70 rays) (Fig. 3, Table 2). Pelvic fins had only one ray during the preflexion stage (2.8 mm SL) (Fig. 1a), increasing to three rays during flexion (Fig. 1b), and were completely formed with six rays (Table Fig. 4. – Symphurus trewavasae larval development: (a): preflexion 2) at the beginning of the postflexion stage (Fig. 3). larvae (2.8 mm NL); (b): larvae in flexion (5.8 mm SL); (c): post- The only elongated fin ray was the third ray of this fin flexion larvae (8.6 mm SL) and (d): metamorphosis larvae (10.5 (Fig. 1c). The development of the anal fin began at mm SL). the flexion stage and attained its final number of rays remained similar with the increment of body size and (65-66) (Table 2) at the beginning of the postflexion the eyes were very small. The intestine was noticeably stage (Fig. 3). The caudal fin had 10-17 rays during the coiled in all developmental stages. The gas bladder was flexion stage (Fig. 3) and reached its definitive number heavily pigmented, with three or four distinct melano- (17 rays) in the postflexion stage (Table 2). The pecto- phores (Fig. 4a-d). ral fin ossification was not complete at the end of the At the preflexion stage (2.8-3.7 mm NL), there postflexion stage (Figs. 1c, 3). were three dash-like clusters of pigment along the dorsal margin of the body between myomers 7-10, 17-19 Symphurus trewavasae and 29-31 (Fig. 4a). One melanophore per myomer, from myomer 11 to approximately 49, was observed General morphological features and pigmentation on the ventral margin of the tail (Fig 4a). Four internal melanophores appeared above the hindbrain before the The smallest larva collected (preflexion larva) was insertion of the elongated rays of the dorsal fin (Fig 2.8 mm NL. In all developmental stages the larval body 4a). One melanophore was found at the base of the was compressed and ribbon-like. The body depth (BD) pectoral fin (Fig 4a-b).

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Fig. 5. – Regression between (a): body depth (BD); (b): head length (HL); (c): preanal length (PAL) and notochordal length (NL) or standard length (SL); and between (d): head depth (HD) and head length (HL) of Symphurus trewavasae larvae. Values in parenthesis are 95% CI of the slope.

Notochord flexion started at 5.9 mm and was com- During metamorphosis, larval pigmentation was pleted at 7.4 mm SL (flexion stage). There were five lost and the adult pigmentation developed. At the be- dash-like clusters of pigment along the dorsal margin ginning of this stage, the pigmentation intensified over of the body between myomers 3-5, 12-16, 24-27, 33- the cephalic region. Pigmentation along the ventral 39 and 44-45 (Fig. 4b). Along the ventral margin of margin of the tail became more continuous and series the tail, three dash-like clusters of pigment were ob- of internal pigments appeared along the vertebral col- served between myomers 8-17, 25-30 and 36-39 (Fig. umn in the posterior half of the body. Along the dorsal 4b). There were four internal melanophores above the margin of the tail, there were four dash-like clusters hindbrain under the insertion of the elongated rays of of pigment between myomers 4-8, 14-16, 31-36 and the dorsal fin (Fig 4b). 52-55, and there were two small melanophores on the At the postflexion stage (8.3-9.3 mm SL), the gut distal tips of dorsal pterygiophores 33 and 34 (Fig. was relatively shorter than before. Several melano- 4d). Two groups of small pigments were also observed phores were present along the ventral and lateral sur- on the dorsal fin between rays 52-55 and 68-75, and face of the abdomen, which increased in pigmentation another group on the anal fin between rays 20 and 28 with larval size (Fig. 4c-d). There were four dash-like (Fig. 4d). clusters of pigment along the dorsal margin of the body between myomers 1-3, 12-16, 27-30 and 41-43. Few melanophores were observed on the ventral margin of the tail, with the consequent formation of three main groups. The first group consisted of four melanophores between myomers 13 and 16, the other two groups were composed of three melanophores located between myomers 28-30 and 40-42 respectively (Fig. 4c). There were two small melanophores on the distal tips of dorsal pterygiophores 56 and 57, and two of them on the distal tips of ventral pterygiophores 35 and 36 (Fig. 4c). Migration of the right eye was completed in the metamorphic stage (it started at 10.5 mm SL), leaving Fig. 6. – Sequence of the development of morphological characters both eyes to the left side of the head. The gut became in early life stages of Symphurus trewavasae in relation to notochordal length (NL) or standard length (SL): start of development of shorter and more heavily pigmented (Fig. 4d). The the character ( ); appearance of fin rays ( ); character protruding gut was incorporated into the ventral body completely developed ( ). Pref. stage: preflexion stage; Post. profile (Fig. 4d). stage: postflexion stage; Meta. stage: metamorphosis stage.

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Table 3. – Sequence of appearance and number of myomeres, vertebrae and fin rays of Symphurus trewavasae larvae. Body length (mm) Larval stages Total myomeres Total vertebrae Dorsal rays Anal rays Pelvic rays Caudal rays 2.8 Preflexion 47 3.3 Preflexion 46 4 3.3 Preflexion 45 4 3.3 Preflexion 47 3.7 Preflexion 48 4 3.7 Preflexion 5.1 Flexion 45 45 84 68 5 6.2 Flexion 48 37 85 71 7 6.3 Flexion 48 45 86 72 7 6.6 Flexion 48 48 87 72 8 7.0 Flexion 48 48 89 76 4 10 7.3 Flexion 48 48 88 73 4 10 7.3 Flexion 49 49 82 74 4 10 7.4 Flexion 50 50 86 75 10 8.3 Postflexion 48 48 90 75 4 10 8.6 Postflexion 48 48 91 77 4 10 9.3 Postflexion 49 49 87 70 4 10 10.5 Metamorphosic 49 49 90 74 4 10

Table 1 includes the indices related to SL that most (Fig. 6, Table 3). The pectoral fins were reabsorbed at clearly represent the body transformation, and Fig. metamorphosis (Figs. 4d, Fig. 6). 5 shows the morphometric regressions. Symphurus trewavasae larvae were moderately elongate during all DISCUSSION their development. BD and HL growth was isometric throughout larval development (P>0.05) (Figs. 5a and In this description, the main identification charac- 5b respectively). PAL increased with respect to SL, fol- ters, such as the meristic characteristics and pigmenta- lowing a negative allometric growth pattern (P<0.05) tion pattern, were analyzed so that Etropus longimanus (Fig. 5c), decreasing from 55.5% NL to 32.5% SL in and Symphurus trewavasae larvae can be recognized. fish up to 10 mm SL (Table 1). HD increased isometri- In general, species of the genus Etropus have 2 cally with respect to HL (P>0.05) (Fig. 5d). or 3 elongated rays on the dorsal fin (Ahlstrom et al. 1984). In this study we detected 2 rays on the dorsal Fins and meristic features fin and 1 on the pelvic fins. Tucker (1982) found the same number of elongated rays; however, they were at The examined specimens of Symphurus trewavasae the second and third positions on the dorsal fin and the had a total of between 45 and 50 myomers (mode: 48 second position on the ventral fin. Only one species of myomers). Vertebral column ossification started previ- Etropus, E. longimanus, is recognized on the Argen- ously. A total of 48-50 vertebrae (without urostyle ) tine continental shelf (Cousseau and Denegri 1997). was recorded in 6.6-7.4 mm SL flexion larvae (mode Although the general pigmentation pattern ob- 48 vertebrae) (Fig. 6, Table 3). The interdigitation pat- served in Etropus longimanus was similar to that found tern of the tonguefish species was 1-3-2-2-2 (100%, for most of the species of these genera (Ahlstrom et al. n=10). 1984), during the preflexion stage, internal notochordal pigment consisted of a series of three fine dashes along Fin development the dorsal surface and was shorter than the pattern observed by Tucker (1982) in Etropus crossotus. In At the beginning of the preflexion stage, finfold and E. crossotus, some pigments were observed on each pectoral fin buds were present (Figs. 4a, Fig. 6). The side of the symphysis of the lower jaw, the posterior finfold was gradually lost (Figs. 4b, 4c, 6). Dorsal fin margin of the articular and at the junction of the left development began in preflexion larvae (3.3 mm NL) and right branchiostegal membranes (Tucker 1982), with four elongated rays at the start of the dorsal fin, but in E. longimanus, there were only a few internal which remained to the postflexion stage (Fig. 4a-c). melanophores over the hindbrain in the head during all The dorsal fin attained the final number of rays (82- the development stages. In E. longimanus no pigments 91) in the postflexion stage (Fig. 6, Table 3). In the were observed in the elongated rays, although Tucker metamorphosis stage, the elongated rays disappeared (1982) found melanophores at the distal end of them. (Fig. 4d). During the flexion stage the anal and caudal The body depth in Etropus longimanus increased fins began developing (6.2 mm SL) (Figs. 4b, 6, Table with size, like E. crossotus larvae from the northeast 3) and reached the final number of rays in specimens of Atlantic and Gulf of Mexico (Tucker 1982). Most 7 mm NL with 70-77 rays in the anal fin and 10 rays in of the other morphometric characters obtained for the caudal fin (Table 3). The development of the pelvic E. longimanus were similar to those observed for E. fins was complete in specimens of 7 mm NL (4 rays) crossotus, except for the preanal length, which grew

SCI. MAR., 76(1), March 2012, 29-37. ISSN 0214-8358 doi: 10.3989/scimar.2012.76n1029 36 • C. DERISIO et al. allometrically in the latter species (Tucker 1982). E. The growth pattern of certain body parts is char- longimanus completed its dorsal, anal and pelvic fins acteristic for the species. In Symphurus trewavasae in the postflexion stage. This was different in E. cros- larvae, head length and body depth followed an sotus, for which Tucker (1982) observed that these fins isometric growth pattern in relation to the SL. Con- were completed at the end of the flexion stage. This versely, S. williamsi showed a negative allometric author observed that the pectoral fins were completely growth pattern (Aceves-Medina et al. 1999). Like S. developed during late metamorphosis. No larvae of williamsi (Aceves-Medina et al. 1999), the preanal E. longimanus in the metamorphic stage were found length followed a negative allometric growth pattern in this study, so we were unable to determine the size in S. trewavasae. at which the development of the pectoral fins was The species of the genus Symphurus may have complete. the first 7 dorsal-fin rays elongated (Evseenko 1990, Notochordal flexion of Etropus longimanus started Aceves-Medina et al. 1999). S. trewavasae only had in smaller larvae in E. crossotus (Tucker 1982). In both four rays, which remained to metamorphosis. S. chaba- E. longimanus and E. crossotus (Tucker 1982), the de- naudi and S. prolatinaris had 2 elongated rays on the velopment of the vertebral column was completed in dorsal fin (second and third) that shortened later in the flexion stage. metamorphic larvae (Evseenko and Shtaut 2000), and Given the high risk of predation on teleost fish lar- S. williamsi had 3 elongated rays (Aceves-Medina et vae, head spines are of great use for defence and are al. 1999). In S. trewavasae, development of the dorsal also considered as diagnostic elements (Neira et al. and anal fins was completed during the flexion stage, 1998). Species of the genus Etropus are characterized followed by the pelvic and caudal fins. This did not by one or more rows of small preopercular spines (Ahl- agree with the studies carried out by Aceves-Medina et strom et al. 1984). According to Tucker (1982), some al. (1999) on S. williamsi, for which the dorsal and anal of the species, such as E. crossotus, have small frontal- fins developed last. The caudal fin is completed in S. sphenotic spines. Preopercular spines were not found williamsi at the beginning of the postflexion stage. The in E. longimanus. The absence of head spines could be pectoral fin is reabsorbed at the end of posflexion stage due to the decalcification of the bony part influencing (Aceves-Medina et al. 1999), and not in the metamor- stained spines and making them hardly visible. Vulner- phic stage, like in S. trewavasae. ability to destruction in the capture, fixation and pres- The range of the total number of myomeres in ervation processes also needs to be considered (Munoz Symphurus trewavasae (45-50) matched the number of et al. 1988). vertebrae reported for juveniles (Derisio 2004). In S. Previous studies have indicated the problems in- williamsi (Aceves-Medina et al. 1999) the full comple- volved in identifying Symphurus species with over- ment of vertebrae was recorded in the preflexion stage. lapping meristic and morphometric characteristics In S. trewavasae, this occurred in the flexion stage. (Munroe 1992, Saldierna-Martinez et al. 2010). There Although it is difficult to identify the larvae of the are two species of Symphurus that inhabit the waters species of the genera Etropus and Symphurus, the best off Buenos Aires. These two species have different characters for confidently identifying larvae to species meristic characters. Symphurus jenynsi, has 59 total level are the number of elongate dorsal rays and the vertebrae while Symphurus trewavasae has only 49 number of vertebrae. The interdigitation pattern can (Derisio 2004). The predominant interdigitation pattern also be considered to identify Symphurus spp. observed in this study coincided with one of the variant patterns found by Munroe (1992) in S. trewavasae. ACKNOWLEDGEMENTS Symphurus trewavasae from southern Brazil (23- 29°S), described by Kurtz and Matsuura (1994), was We thank the crew and onboard scientific staff for very similar to our description. The main difference collecting the material. We also thank the Scientific was the developmental time of the caudal and ven- Editor and reviewers of this manuscript for provid- tral fins, observed in the postflexion stage by these ing useful comments that considerably improved the authors. The differences detected in the two studies manuscript. This is an INIDEP Contribution Nº 1684. could be due to the different latitudinal distributions of the two groups. REFERENCES In Symphurus trewavasae, the flexion stage began at 5.9 mm NL and finished at 7.4 mm SL like S. williamsi Aceves-Medina G., Gonzalez E.A., Saldierna R.J. 1999. Larval development of Symphurus williamsi (Cynoglossidae: Pleuronec- (Aceves-Medina et al. 1999). The size of the specimens tiformes) from the Gulf of California. Fish. Bull. 97: 738-745. at the time of metamorphosis varied between species. Ahlstrom E.H., Amaoka K., Hensley DA., Moser H.G., Sumida BY. In S. trewavasae and S. williamsi, this stage began at 1984. Pleuronectiformes: Development. In: Moser G., Richards W.J., Cohen D.M., Fahay M.P., Kendall A.W., Richardson S.L. 10.5 mm SL (Aceves-Medina et al. 1999), whereas (eds.), Ontogeny and Systematics of Fishes. Am. Soc. Ichthyol. in other species of this genus, such as S. chabanaudi 1: 670-687. and S. prolatinaris, this process occurred later (15.3 Cousseau M.B., Denegri M.A. 1997. Peces. In: Cousseau M.B. mm SL and 19.6 mm SL respectively) (Evseenko and (ed.), Peces, crustáceos y moluscos registrados en el sector del Atlántico Sudoccidental comprendido entre 34° y 55° S, con Shtaut 2000). indicación de las especies de interés pesquero. INIDEP INF.

SCI. MAR., 76(1), March 2012, 29-37. ISSN 0214-8358 doi: 10.3989/scimar.2012.76n1029 E. LONGIMANUS AND S. TREWAVASAE LARVAL DEVELOPMENT • 37

TEC. 5: 9-47, Mar del Plata. Munroe T.A. 1998. Systematics and ecology of tonguefishes of the Derisio C. 2004. Descripción de larvas y juveniles de Pleuronecti- genus Symphurus (Cynoglossidae: Pleuronectiformes) from the formes en el Mar Argentino. Tesis de Licenciatura. Univ. Mar western Atlantic Ocean. Fish. Bull. 96: 1-182. del Plata, 72 pp. Munoz H., Herrera G., Fuentes H. 1988. Desarrollo larval del lenguado Diaz de Astarloa J.M. 2002. The flatfish fisheries on both sides of de ojos chicos Paralichthys microps. Rev. Biol. Mar. 24: 37-53. the Atlantic Ocean. Thalassas. 18: 67-82. Neira F.J., Miskiewicz A.G., Trnski T. 1998. Larvae of temperate Evseenko S.A. 1990. Unusual larvae of the marine tonguefish, Sym- Australian fishes. Laboratory guide for larval fish identifica- phurus sp. (Cynoglossidae), from central waters of the eastern tion. University of Western Australia Press, 474 pp. Pacific. J. Ichthyol. 30: 148-154. Traslated from Vopr. Ihtiol, Nellen W., Hempel G. 1969. Versuche zur Fangigkeit des «Hai» 30: 682-686. und des modifizierten Gulf-V-plankton-sampler «Nackthai». Evseenko S.A., Shtaut M.I. 2000. Early stages of development of Meeresforsch. 20: 141-154. two species of tongue soles- Symphurus chabanaudi and S. Potthoff T. 1984. Clearing and staining techniques. In: Moser G., prolatinaris (Cynoglossidae, Pleuronectiformes) from central Richards W.J., Cohen D M., Fahay MP., Kendall A.W., Rich- eastern Pacific. Vopr. Ihtiol. 40: 792-803. ardson S.L. (eds.), Ontogeny and Systematics of Fishes. Am. Fabré N.N., Diaz de Astarloa J.M. 1996. Pleuronectiformes de Soc. Ichthyol. 1: 35-37. importancia comercial en el sector del Atlántico Sudoccidental Saldierna-Martínez R.J., Aceves-Medina G., González-Navarro comprendido entre los 34o 30’ y 55oS. Distribución y considera- E.A. 2010. Larval development of the sportfin tonguefish (Sym- ciones sobre la pesca. Rev. Inv. Des. Pesq. 10: 45-55. phurus oligomerus) (Pleuronectiformes: Cynoglossidae) from Fabré N.N., Díaz de Astarloa J.M. 2001. Distributional patterns and the Gulf of California, México. Fish. Bull. 108: 45-55. abundance of paralichthyid flounders in the South-west Atlantic Sumida B.Y., Ahlstrom E.H., Moser H.G. 1979. Early development (Pleuronectiformes: Paralichthyidae). Thalassas. 17: 45-55. of seven flatfishes of the eastern North Pacific with heavily Figueiredo J.L., Menezes N.A. 2000. Manual de peixes marinhos pigmented larvae (Pisces, Pleuronectiformes). Fish. Bull. 77: do sudeste do Brasil. VI. Teleostei (5). Mus. Zool. Univ. Sao 105-145. Paulo, 116 pp. Taylor W.R., Van Dyke G.C. 1985. Revised procedures for stain- Kurtz F.W., Matsuura Y. 1994. Early development of four tongue- ing and clearing small fishes and other vertebrates for bone and fishes of the Genus Symphurus (Osteichthyes: Cynoglossidae) cartilage study. Cybium 9: 107-119. from the Southern Brazil. Jpn. J. Ichthyol. 41: 141-148. Trnski T., Leis T.M. 1991. A beginner’s guide to illustrating fish Menezes N., Benvegnu G.Q. 1976. On the species of the genus larvae. In: Hancock D. A. (ed.), Larval Biology. Bur. Rural Re- Symphurus from the Brazilian coast, with descriptions of two sour. Proc. Australian Government Printing Office, Canberra. new species (Osteichthyes, Pleuronectiformes, Cynoglossidae). 15: 198-202. Pap. Avulsos. Zool. 30: 137-170. Tucker J.W. 1982. Larval development of Citharichthys cornutus, Menni R.C., Ringuelet R.A., Aramburu R.H. 1984. Peces marinos de C. gymnorhinus, C. spilopterus, and Etropus crossotus (Bothi- la Argentina y Uruguay. Hemisferio Sur, Buenos Aires, 359 pp. dae), with notes on larval occurrence. Fish. Bull. 80: 35-73. Munroe T.A. 1992. Interdigitation pattern of dorsal-fin pterigi- ophores and neural spines, an important diagnostic for Sym- Scient. ed.: M.P. Olivar. phurine tongues fishes (Symphurus: Cynoglossidae: Pleuronec- Received October 19, 2010. Accepted May 25, 2011. tiformes). Bull. Mar. Sci. 50: 357-403. Published online October 28, 2011.

SCI. MAR., 76(1), March 2012, 29-37. ISSN 0214-8358 doi: 10.3989/scimar.2012.76n1029